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Carbon processing by the benthic ecosystem and benthic C fixation in methane-rich sediments on the South Georgia margin

Published online by Cambridge University Press:  18 March 2019

Clare Woulds Open the ORCID record for Clare Woulds [Opens in a new window] ,
James B. Bell ,
Adrian G. Glover ,
Steven Bouillon  and
Louise S. Brown
Clare Woulds*
Affiliation:
School of Geography, University of Leeds, Leeds LS2 9JT, UK
James B. Bell
Affiliation:
School of Geography, University of Leeds, Leeds LS2 9JT, UK Cefas, Pakefield Road, Lowestoft, NR33 0HT, UK
Adrian G. Glover
Affiliation:
Life Sciences Dept., Natural History Museum, Cromwell Rd, London SW7 5BD, UK
Steven Bouillon
Affiliation:
Department of Earth and Environmental Sciences, KU Leuven, Leuven, Belgium
Louise S. Brown
Affiliation:
School of Geography, University of Leeds, Leeds LS2 9JT, UK Cefas, Pakefield Road, Lowestoft, NR33 0HT, UK
*
[email protected]
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Abstract

As bottom water warms, destabilisation of gas hydrates may increase the extent of methane-rich sediments. The authors present an assessment of organic carbon processing by the benthic community in methane-rich sediments, including one of the first investigations of inorganic C fixation in a non-hydrothermal vent setting. This topic was previously poorly studied, and there is much need to fill the gaps in knowledge of such ecosystems. The authors hypothesized that benthic C fixation would occur, and that a high biomass macrofaunal community would play a substantial role in organic C cycling. Experiments were conducted at a 257 m deep site off South Georgia. Sediment cores were amended with 13C and 15N labelled algal detritus, or 13C labelled bicarbonate solution. In the bicarbonate experiment, labelling of bacteria-specific phospholipid fatty acids provided direct evidence of benthic C fixation, with transfer of fixed C to macrofauna and dissolved organic carbon (DOC). In the algae experiment, macrofauna played an active role in organic carbon cycling. Compared to similar experiments, low temperature supressed the rates of community respiration and macrofaunal C uptake. While benthic C fixation occurred, the biological processing of organic carbon was dominantly controlled by low temperature and high photic zone productivity.

Keywords

13Ccarbon cyclechemosynthesisisotope tracermacrofaunaseep
Type
Biological Sciences
Information
Antarctic Science , Volume 31 , Issue 2 , April 2019 , pp. 59 - 68
Copyright
Copyright © Antarctic Science Ltd 2019 

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References

Bell, J.B., Aquilina, A., Woulds, C., Glover, A.G., Little, C.T.S., Reid, W.D.K., et al. 2016. Geochemistry, faunal composition and trophic structure in reducing sediments on the south-west South Georgia margin. Royal Society Open Science, 3, 10.1098/rsos.160284.Google Scholar
Bell, J.B., Woulds, C. & Oevelen, D.V. 2017. Hydrothermal activity, functional diversity and chemoautotrophy are major drivers of seafloor carbon cycling. Scientific Reports, 7, 12025.Google Scholar
Bernardino, A.F., Levin, L.A., Thurber, A.R. & Smith, C.R. 2012. Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. PloS One, 7, e33515.Google Scholar
Boschker, H.T.S. & Middelburg, J.J. 2002. Stable isotopes and biomarkers in microbial ecology. FEMS Microbiology Ecology, 40, 85–95.Google Scholar
Boschker, H.T.S., Vasquez-Cardenas, D., Bolhuis, H., Moerdijk-Poortvliet, T.W.C. & Moodley, L. 2014. Chemoautotrophic carbon fixation rates and active bacterial communities in intertidal marine sediments. PloS One, 9, 10.1371/journal.pone.0101443.Google Scholar
Buhring, S.I., Lampadariou, N., Moodley, L., Tselepides, A. & Witte, U. 2006. Benthic microbial and whole-community responses to different amounts of 13C-enriched algae: in situ experiments in the deep Cretan Sea (Eastern Mediterranean). Limnology and Oceanography, 51, 157–165.Google Scholar
Burdige, D.J., Berelson, W.M., Coale, K.H., Mcmanus, J. & Johnson, K.S. 1999. Fluxes of dissolved organic carbon from California continental margin sediments. Geochimica et Cosmochimica Acta, 63, 1507–1515.Google Scholar
Ciais, P., Sabine, C., Bala, G., Bopp, L., Brovkin, V., Canadell, J., et al. 2013: Carbon and other biogeochemical cycles. In Stocker, T.F., Qin, D., Plattner, G.-K., Tignor, M., Allen, S.K., Boschung, J., et al. , eds. Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press, 1552 pp.Google Scholar
Cook, P.L.M., Veuger, B., Boer, S. & Middelburg, J.J. 2007. Effect of nutrient availability on carbon and nitrogen incorporation and flows through benthic algae and bacteria in near-shore sandy sediment. Aquatic Microbial Ecology, 49, 165–180.Google Scholar
Del Giorgio, P.A. & Cole, J.J. 1998. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology and Systematics, 29, 503–541.Google Scholar
De Troyer, I., Bouillon, S., Barker, S., Perry, C., Coorevits, K. & Merckx, R. 2010. Stable isotope analysis of dissolved organic carbon in soil solutions using a catalytic combustion total organic carbon analyzer-isotope ratio mass spectrometer with a cryofocusing interface. Rapid Communications in Mass Spectrometry, 24, 365–374.Google Scholar
Gontikaki, E., Van Oevelen, D., Soetaert, K. & Witte, U. 2011. Food web flows through a sub-Arctic deep-sea benthic community. Progress in Oceanography, 91, 245–259.Google Scholar
Guezennec, J. & Fialamedioni, A. 1996. Bacterial abundance and diversity in the Barbados Trench determined by phospholipid analysis. FEMS Microbiology Ecology, 19, 83–93.Google Scholar
Hunter, W.R., Jamieson, A., Huvenne, V.A.I. & Witte, U. 2013. Sediment community responses to marine vs terrigenous organic matter in a submarine canyon. Biogeosciences, 10, 67–80.Google Scholar
Hunter, W.R., Levin, L.A., Kitazato, H. & Witte, U. 2012. Macrobenthic assemblage structure and organismal stoichiometry control faunal processing of particulate organic carbon and nitrogen in oxygen minimum zone sediments. Biogeosciences, 9, 993–1006.Google Scholar
Levin, L.A. 2005. Ecology of cold seep sediments: interactions of fauna with flow, chemistry and microbes. In Gibson, R.N., Atkinson, R.J.A. & Gordon, J.D.M., eds. Oceanography and Marine Biology: an Annual Review. Vol. 43. Boca Raton, FL: CRC Press, 1–46.Google Scholar
Levin, L.A. & Michener, R.H. 2002. Isotopic evidence for chemosynthesis-based nutrition of macrobenthos: the lightness of being at Pacific methane seeps. Limnology and Oceanography, 47, 1336–1345.Google Scholar
Main, C.E., Ruhl, H.A., Jones, D.O.B., Yool, A., Thornton, B. & Mayor, D.J. 2015. Hydrocarbon contamination affects deep-sea benthic oxygen uptake and microbial community composition. Deep-Sea Research I: Oceanographic Research Papers, 100, 79–87.Google Scholar
Molari, M., Manini, E. & Dell'anno, A. 2013. Dark inorganic carbon fixation sustains the functioning of benthic deep-sea ecosystems. Global Biogeochemical Cycles, 27, 212–221.Google Scholar
Moodley, L., Middelburg, J.J., Boschker, H.T.S., Duineveld, G.C.A., Pel, R., Herman, P.M. & Heip, C.H.R. 2002. Bacteria and foraminifera: key players in a short-term deep-sea benthic response to phytodetritus. Marine Ecology Progress Series, 236, 23–29.Google Scholar
Moodley, L., Middelburg, J.J., Soetaert, K., Boschker, H.T.S., Herman, P.M. & Heip, C.H.R. 2005. Similar rapid response to phytodetritus deposition on shallow and deep-sea sediments. Journal of Marine Research, 63, 457–469.Google Scholar
Pond, D.W., Bell, M.V., Dixon, D.R., Fallick, A.E., Segonzac, M. & Sargent, J.R. 1998. Stable-carbon-isotope composition of fatty acids in hydrothermal vent mussels containing methanotrophic and thiotrophic bacterial endosymbionts. Applied and Environmental Microbiology, 64, 370–375.Google Scholar
Pozzato, L., Cathalot, C., Berrached, C., Toussaint, F., Stetten, E., Caprais, J.C., et al. 2017. Early diagenesis in the Congo deep-sea fan sediments dominated by massive terrigenous deposits: part I - oxygen consumption and organic carbon mineralization using a micro-electrode approach. Deep-Sea Research II: Topical Studies in Oceanography, 142, 125–138.Google Scholar
Pruski, A.M., Decker, C., Stetten, E., Vetion, G., Martinez, P., Charlier, K., et al. 2017. Energy transfer in the Congo deep-sea fan: from terrestrially-derived organic matter to chemosynthetic food webs. Deep-Sea Research II: Topical Studies in Oceanography, 142, 197–218.Google Scholar
Rabouille, C., Olu, K., Baudin, F., Khripounoff, A., Dennielou, B., Arnaud-Haond, S., et al. 2017. The Congolobe project, a multidisciplinary study of Congo deep-sea fan lobe complex: overview of methods, strategies, observations and sampling. Deep-Sea Research II: Topical Studies in Oceanography, 142, 7–24.Google Scholar
Romer, M., Torres, M., Kasten, S., Kuhn, G., Graham, A.G.C., Mau, S., et al. 2014. First evidence of widespread active methane seepage in the Southern Ocean, off the sub-Antarctic island of South Georgia. Earth and Planetary Science Letters, 403, 166–177.Google Scholar
Rossi, F. 2007. Recycle of buried macroalgal detritus in sediments: use of dual-labelling experiments in the field. Marine Biology, 150, 1073–1081.Google Scholar
Treude, T., Boetius, A., Knittel, K., Wallmann, K. & Jorgensen, B.B. 2003. Anaerobic oxidation of methane above gas hydrates at Hydrate Ridge, NE Pacific Ocean. Marine Ecology Progress Series, 264, 1–14.Google Scholar
Sweetman, A.K., Smith, C.R., Shulse, C.N., Maillot, B., Lindh, M., Church, M.J., et al. In press. Key role of bacteria in the short-term cycling of carbon at the abyssal seafloor. Limnology and Oceanography.Google Scholar
Van Oevelen, D., Soetaert, K., Middelburg, J.J., Herman, P.M.J., Moodley, L., Hamels, I., et al. 2006. Carbon flows through a benthic food web: integrating biomass, isotope and tracer data. Journal of Marine Research, 64, 453–482.Google Scholar
Veuger, B., Middelburg, J.J., Boschker, H.T.S. & Houtekamer, M. 2005. Analysis of 15N incorporation into D-alanine: a new method for tracing nitrogen uptake by bacteria. Limnology and Oceanography: Methods, 3, 230–240.Google Scholar
Witte, U., Aberle, N., Sand, M. & Wenzhofer, F. 2003a. Rapid response of a deep-sea benthic community to POM enrichment: an in situ experimental study. Marine Ecology Progress Series, 251, 27–36.Google Scholar
Witte, U., Wenzhofer, F., Sommer, S., Boetius, A., Heinz, P., Aberle, N., et al. 2003b. In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor. Nature, 424, 763–766.Google Scholar
Woulds, C., Andersson, J.H., Cowie, G.L., Middelburg, J.J. & Levin, L.A. 2009. The short-term fate of organic carbon in marine sediments: comparing the Pakistan margin to other regions. Deep Sea Research II: Topical Studies in Oceanography, 56, 393–402.Google Scholar
Woulds, C., Bouillon, S., Cowie, G., Drake, E., Middelburg, J.J. & Witte, U. 2016. Patterns of carbon processing at the seafloor: the role of faunal and microbial communities in moderating carbon flows. Biogeosciences, 13, 3343–4357.Google Scholar
Woulds, C., Cowie, G.L., Levin, L.A., Andersson, J.H., Middelburg, J.J., Vandewiele, S., et al. 2007. Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling. Limnology and Oceanography, 52, 1698–1709.Google Scholar
Yamanaka, T. & Sakata, S. 2004. Abundance and distribution of fatty acids in hydrothermal vent sediments of the western Pacific Ocean. Organic Geochemistry, 35, 573–582.Google Scholar
Zhang, C.L., Huang, Z.Y., Cantu, J., Pancost, R.D., Brigmon, R.L., Lyons, T.W. & Sassen, R. 2005. Lipid biomarkers and carbon isotope signatures of a microbial (Beggiatoa) mat associated with gas hydrates in the Gulf of Mexico. Applied and Environmental Microbiology, 71, 2106–2112.Google Scholar